Helminth parasites (Plathelminthes) of common carp (Cyprinus carpio L.) in Iznik Lake

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1 Bull. Eur. Ass. Fish Pathol., 22(5) 2002, 343 Helminth parasites (Plathelminthes) of common carp (Cyprinus carpio L.) in Iznik Lake Ali Aydogdu* & F. Naci Altunel Uludag University, Science Faculty, Department of Biology, Bursa-TURKEY Abstract Occurrence of plathelminth parasites of common carp in Iznik Lake was investigated monthly from February 1995 to January A total of 145 common carp were caught and 115 specimens of host were infected with 3 species of plathelminth parasites: Dactylogyrus extensus (Monogenea), Caryophyllaeus laticeps (Cestoda) and Bothriocephalus acheilognathi (Cestoda). The dominant parasite species D. extensus was occurred on host gills throughout the year. Total prevalence of D. extensus was 69.7% This species was the most prevalent found in fish and the infection was the highest in May. C. laticeps was the second dominant parasite in this study. A total of 740 parasites were found and no parasite specimens was found on fish form July until November. The infection rate was the highest in March. And total prevalence of C. laticeps was 29 %. B. acheilognathi was found in 18 of the 145 fish examined. Fifty fish containing a total of 293 parasites were found. B. acheilognathi infection rate was the highest during Autumn and Summer (especially in June) and the lowest during Spring. The total prevalence was 12.4 %. Intensity, seasonal changes of the parasite species are discussed in detail. The common carp (Cyprinus carpio L.) was introduced to Turkey at the beginning of 1900s and was bred in aquaculture systems until the middle of last century. Successful natural reproduction of the carp occurs sporadically in Turkey now. Therefore, carp in the coloured koi variety is common and important for aquarium and pond use. The helminth fauna of the common carp in Turkey was investigated by Oguz, (1991), Oguz et al. (1996), Aydogdu (1997), Becer and Kara (1998). Among the ectoparasites of the common carps, two species of monogenean parasites, Dactylogyrus sp. and Dactylogyrus extensus, were collected at the Bursa region (Kocadere- Ekinli and Uluabat) (Oguz, 1991), Uluabat Lake (Oguz et al. 1996). Crustacea was the second group of ectoparasites of the common group examined in Turkey. Two species of Crustacea, Ergasilus sp., Argulus foliaceus, were collected from fresh water of Bursa region (Kocadere-Ekinli and Uluabat) (Oguz, 1991) and Iznik Lake (Aydogdu 1997). The endoparasite fauna was found to be more diverse. Species of three genera of Cestoda Bothriocephalus sp. from Uluabat Lake (Oguz et al. 1996), B. acheilognathi from Kovada Lake (Becer and Kara, 1998), Caryophyllaeus laticeps from Kovada Lake (Becer and Kara, 1998), Ligula intestinalis from Kovada Lake (Becer and Kara, 1998) and one genus of Acanthocephala, Neoechinohychus rutili, from Iznik Lake (Aydogdu, 1997) were determined in Turkey. The present study aims to increase our knowledge on the occurrence of parasites of the common carp in a different locality in Turkey.

2 Bull. Eur. Ass. Fish Pathol., 22(5) 2002, 344 Month Feb Mar Apr May The fish examined were from Iznik Lake, about 75 km south - east of Istanbul. The lake is 32 km long and 12 km wide and is the biggest freshwater lake of South Marmara Region. During the year of this study monthly water temperature was highest in June (Mean 28 C, range 24 C to 32 C ) and lowest in January (Mean 7 C, range 4 C to 12 C ) study has been done water temperature in the averages in ranging from 7,3 C to 28 C. The fish population was investigated between February 1995 and January 1996 in monthly samples. During this study, the carp were caught using net, hook or blow net. The fish were always transported to the laboratory alive, in aerated cans or polyethylene bags inflated with oxygen. When the sampling was performed in summer, the water used for transporting the fish to the laboratory was cooled with ice. Fish were placed in flow through type concrete basins and aquaria in the laboratory, and dissected as soon as possible, within few days after sampling. The fish were examined for the presence of plathelminth parasites. The dissection of organs were done under stereomicroscope and light microscope equipped with phase contrast. The parasite specimens were fixed in formaldehyde or Jun No of carp examined No. of infected carp Jul Aug Sep Oct Nov Dec Jan Total D. extensus C. laciteps B. acheilognathi Prevalence D. extensus of infected C. laciteps carp B. acheilognathi No. of worms found D. extensus C. laciteps B. acheilognathi Table 1. Plathelminth in Common carp (Cyprinus carpio L.) in Iznik lake between February 1995 and January Bouin s fluid stained with Mayer s haematoxylin. Then, the specimens were kept in canada balsam and dehydrated through an ethanol series: 70 % ethanol for (15-20 minute ), 80 % ethanol (10 minute ), 90% ethanol (5 minute ), and 100 % ethanol (5 minute) and finally two minutes in xylol. All the parasites found were counted and identified (Table 1). The taxonomical determination were done according to Markevic (1951), Yamaguti (1961, 1963), Bychovskaya - Pavkoskava (1964) and Gussev ( 1985). We examined 145 specimens of the common carp in the Iznik Lake. One species of ectoparasites on gills, D. extensus, and two endoparasite species, C. laticeps, B. acheilognathi, parasitising in intestine of the common carp were recorded. The dominant parasite species was D. extensus being the most frequent and numerous species. This species was recorded on the common carp throughout the year. The infection was the highest in May Of 145 fish examined, 101 were infected by D. extensus (Total prevalence 69.7%). A total of 2871 parasites were found on 101 fish (Table 1). While prevalence of D. extensus increased sharply from August

3 Bull. Eur. Ass. Fish Pathol., 22(5) 2002, 345 to November, Prevalence peaked in May and June. The sharp increases was recorded in December again. Changes in intensity of D. extensus followed a seasonal pattern in year of the study. While the highest intensity were observed in May, the lowest level in intensity were recorded in February. Two different types of Cestoda were found in the present study and were identified as C. laticeps and B. acheilognathi. The second dominant species was C. laticeps. A total of 740 parasites were found. The infection of C. laticeps exhibited an obvious seasonal cycle (Table 1). No parasite specimen was found on the common carp from July until November. The infection of C. laticeps occurred in November and rapidly increased in March. The decline of C. laticeps infection was recorded in April and total disappearance of this parasite species from common carp was in July. The prevalence of C. laticeps peaked in February and January, then sharply decreased in April. A total of 293 specimens of B. acheolognathi were found in intestine of host fish. The infection of B. acheilognathi was encountered in intestine in spring, summer and autumn. The highest infection (prevalence and intensity) occurred in June (Table1). The occurrence of several species of plathelminth parasites of the common carp was observed in the Iznik Lake, Turkey. Altogether, three species of plathelminths, D. extensus, C. laticeps and B. acheilognathi were found. The present data show that D. extensus infection is optimal during spring and summer, however infestation by this parasites occurred throughout year. Dactylogyrus lay eggs on fish gills or in water, where they fall to the bottom of the reservoir. Egg development depends on external conditions, primarily on temperature, e.g., in Summer at C, D. vastator larvae develop and hatch in 2 3 days, at 18 C larval development takes approximately a month in water when water temperatures fall below 4 C no changes can be observed in eggs, with development only commencing when the temperature rises (Markewich, 1951). The data from the lake Iznik seem to support the link with water temperature: In lake Iznik, the peak of infection of D. extensus from May to July corresponds with increasing water temperature, and the decline in infection by D. extensus decreased during winter and autumn, coinciding with the decline of water temperature. This may be explained by the report that D. extensus is a thermophilic parasite with a shorter life cycle at higher temperatures (Silvia et al., 1991, Kritscher 1982, 1988, Pojmanska 1995) which could explain the dominance of this species in summer months. The present study supports the data in the literature concerning the dynamics of the occurrence of this monogenean species. C. laticeps is a characteristic common parasite of cyprinid fishes in Europe. C. laticeps showed some seasonal fluctuations of its infection in fish. In lake Iznik, parasites occurred mainly from November to June causing Autumn and Spring peak of infection. The experimental studies of Kulakovskaja 1962, 1964 showed that C. laticeps larvae preserve their infectivity for fish for up to two years. Depending on the length of the life of their intermediate host, infectivity of procercoids may result in their ability to infect fishes throughout the year. The cyclic character of

4 Bull. Eur. Ass. Fish Pathol., 22(5) 2002, 346 incidence and maturation of these tapeworms in fishes has been widely recorded. Three main factors were regarded as controlling these processes; variations in the availability in the physiological state of host, including the hormone level connected with spawning and resistance of host to infection (Kennedy 1968, 1969). C. laticeps is also affected by a temperature dependent resistance response in the host, and these are considered major factors responsible for periodicity of the incidence of this tapeworm in fish (Kennedy 1969, 1971, Kennedy and Walker 1969). According to these authors, the lowered host resistance in winter allows the parasites to establish in fish, whereas the growing resistance in summer causes the removal of the tapeworms from the intestine of the host, and precludes the establishment of new parasites in the fish. In this study, the data from Iznik lake seem to support the results of Kennedy (1969,1971), and Kennedy and Walker (1969). However these observations should be supported by detailed immunological studies. The studies of Anderson (1974, 1976) on the population dynamics of C. laticeps in final and intermediate hosts based on field data and a theoretical population model showed three factors responsible for the cyclic changes in the parasite population size; a) final host s feeding behaviour b) egg production by adult worms, causing periodic availability of infective larvae and c) temperature dependent mortality of the parasites within the final host. The data from lake Iznik seem to validate at least the two first factors: In lake Iznik, the peak of infection of C. laticeps in spring corresponds with the increasing feeding activity of common carp after winter starvation. In December, when the second peak of infection occurs in the lake Iznik, a new generation of Tubifex tubifex can already harbour the infective procercoids of C. laticeps which require months for development from egg to infective stage (Kulakovskaja 1962, 1964). Some of the factors such as the availability (seasonal occurrence) of intermediate hosts, tubificids, are currently being investigated in the Iznik Lake. In addition, further investigations are obviously necessary in the Iznik Lake before causes of this seasonal occurrence of C. laticeps can be ascertained. B. acheolognathi commonly referred to as the Asian fish tapeworm, has spread from Asia throughout Europe and parts of North America. This parasite is known to infect over 40 species of fish, mainly Cyprinids ( Riggs and Esch 1987). Species of Bothriocephalus are generally non specific for intermediate hosts. B. claviceps, B. cuspidatus and B. acheilognathi, all parasites of freshwater fish infect a variety of cyclopoid copepods. Seasonal changes in the dynamics of most helminth parasites in aquatic ecosystem may be affected by a wide range factors, of both biotic and abiotic orgin. Perhaps the most significant are normal temperature variations (Aho et al., 1982; Camp et al., 1982) and factors associated with host reproduction (Smith, 1973, Anderson 1976). Granath and Esch(1983) found that growth and development of this parasite was stimulated by temperatures above 25 o C and that temperatures of 25 C to 30 C maximised egg maturation, hatching, and coracidium motility. At temperatures outside that range, these activities were depressed. Temperatures exceeding 35 C caused a decrease in recruitment of this parasite in mosquitofus (Granath and Esch, 1983). Water temperature

5 Bull. Eur. Ass. Fish Pathol., 22(5) 2002, 347 in Iznik Lake is suitable for B. acheilognathi, exceeding 20 C from May through October. The data from Iznik lake seem to support the significance of water temperature, with the peak of infection of B. acheilognathi in Summer and Autumn corresponding with the increased water temperature. B. acheilognathi requires high water temperature for completion of its life cycle (Mark et. al., 1997). Also there was a seasonal change in B. acheolognathi infection. This species disappeared in the winter months which probably corresponds with the reduced consumption of food by carp in this season. The seasonal change in occurrence of B. acheolognathi was clear. Klenov (1972) observed the increase of parasite prevalence in fry of grass carp in Russia between July and August and then the decrease in September October. Marcogliese and Esch (1989) noted also the increase of parasite abundance between May and July,the decrease of infection in August September and the second increase in September-October in Gambusia affino from North Carolina. On the other hand, Granath and Esch (1983) and Riggs and Esch (1987) found the negative correlation between the abundance of B. acheolognathi and water temperature. The present data would appear more supportive of the results of Marcogliese and Esch (1989). References Aho, J. M, J.W. Camp, and G.W. Esch Long-term studies on the population biology of Diplostomulum scheurinji in a thermally altered reservoir. J. Parasitol. 68: Anderson, R, M Population dynamics of the cestoda Caryophyllaeus laticeps (Pallas, 1781) in the bream (Abramis brama L.) Journal of Animal Ecology 43, Anderson, R, M Seasonal variations in the population dynamics of Caryophyllaeus laticeps Parasitology 72, Aydogdu, A., Yildirimhan, H.S., Altunel, F. N Iznik Gölünde Yasayan Sazan Balıkları (C. carpıo) üzerinde Yasayan Bazı Metozoon Parazitler Üzerine Arastırmalar Türkiye Parazitoloji Dergisi 21(4) (in Turkish) (with an English abstract ) Becer A. and Kara D., 1998 Kovada Gölünde Yakalanan Sazan (C. carpıo) Baliklarinin Populasyon Yapisi Ve Paraazitleri Üzerine Bir Arastırma. Türkiye Parazitoloji Dergisi 22(2) (in Turkishwith an English abstract) Bychovskaya-Pavlovskaya, I.E Key to parasites of freshwater fishes of the U.S.S.R., II, Moskova, Leningrad, Trans.Birrow A. and Cale, Z.S. 1964, Israel programme for scientfic, tranlation, Jerusalem, 919 pp. Camp, J.W., J.M, Aho, and G.W. Esch Along- term study or various aspects of the population biology of Ornithodiplostomum ptychocheilus in a south Carolina cooling reserıoir. J. Parasitol. 68: Granath, W. O., J. R. And Esch, G.W., Temparature and other factors in regulations the intrapopulation densities and composition of Bothriocephalus acheilognathi in Cambusia Offinis. Journal Of Parasitology 69: 1, Gussev, A.V Key To Parasites Of The Freshwater Fishes Of The Ussr. Metazoon Parasites. Vol. 2. Publ. House Nauka. Leningrad, 424 pp. Kennedy, C. R, Walker P.J Evidence for an immunite response by dace, Leucıscus leucıscus, to infection by the cestode C. laticeps J. parazit. 55, Kennedy, C. R., Population biology of cestode Caryophyllaeus laticeps Pallas,1781 In Dace, Leuciscus leuciscus Of The River Avon, The Journal Of Parasitology Vol. 54 No. 3 Pp

6 Bull. Eur. Ass. Fish Pathol., 22(5) 2002, 348 Kennedy, C. R., Seasonal incidence and development of the cestoda Caryophyllaeus laticeps in the river Avon. Parasitology, 59, Kennedy, C. R., 1971.The effect of temperature upon the establishment and survial of the cestoda Caryophyllaeus laticeps in Orfe, Leuciscus idus. Parasitology 63, Klenov A.P Seasonal and age dynamics of Bothriocephalus gowkongensis infection in Ctenopharyngodon idella. Byulleten Vsesoyuznogo Instituta Gelmintologii, 8, (In Russian). Kritscher. V. E., Die Fische Des Neusiedlersees Und Ihre Parasiten VII. Trematoda Monogenea Und Zusammen Tassung., Ann. Naturlist. Mus. Wien. 90. B Kritscher. V. E., 1988 Die Fische Des Neusiedlersees Und Ihre Parasiten Vi. (Cestoidea)., Ann. Naturlist. Mus. Wien. 90. B Kulaskowskaya, O. P Development of Caryophylaeidae (Cestoda) in an invertebrate host (Russian text) Zoolgichoskii zhurnal 41, Kulaskowskaya, O. P Life cycles Caryophyllaeidae (Cestoda) in the conditions of western Ukraine (Russian text) Ceskoslovaska parasitolojie 11: Marcogliese D. J., Esch G. W Alterations in seasonal dynamics of Bothriocephalus acheilognathi in a North Carolina cooling reservoir over a seven year period. Journal of Parasitology, 75, M. J. Braunder and T. L. Hoffranle Distribution and prevalence of the Asian fish tapeworm, Bothriocephalus acheilognathi, in the Colorado River and tributorions, Grand Canyon, Arizona. J. Helminthol. Soc. Wash. 64(2) Oguz MC, 1992 in the text is An investigation on carps (Cyprınus carpio L.1758) which were caught from some freshwaters of Bursa region (Kocadere-Ekinli and Uluabat). Türkiye Parazitoloji Dergisi, 15, (2): p (in Turkish). Oguz MC, Öztürk MO, Altunel FN, Ay YD, A parasitological investigation on common carp in Cyprinus carpio L. caught in Uluabat (Apolyont) lake. Türkiye Parazitoloji Dergisi. 20, (1): (in Turkish) Pojmanska, T., Seasonal dynamics of occurrence and some parasites in four Cyprinid fish cultured in ponds. II. Monogenea, Acta Parasitolojica, (1995) 40(2), Rigg,, M. R. and G. W. Esch The Suprapopulation dynamıcs of Bothriocephalus acheilognathi in a north Carolina reservoir: Abudance, dıspersion, and prevalence. J. Parasitology 73: Silvia, L. G G. D. Sepulveda, R. Mercado- Hernandez, J. J. Martinez. and F. Salinas., New localities for monogenetic tremotodes and other ectoparasites of carp (Cyprinus carpio) and catfish Ictalunus puncatus in northeastern Mexico and their relation with some biotic and abiotic factors, The Journal Of The Elisa Mitchall Scientific, 106 (3): Smith, H.D Observations on the cestode Eubothrium solvelini in juvenile sockeye salmon (Oncorhynchus nerka) at Babine Lake, British Columbia, J. Fish. Res. Board. 30: Yamaguti, S Systema Helminthium Cestodes Vol.I, Inter Science Publishers. New York, London,119 pp. Yamaguti, S. 1963: Systema Helminthium Monogenea and Apisdocotylea. Vol.IV, Inter Science Publishers. New York, London, 325pp. Markevic, A. P Parasitic fauna of freshwater of the fish of the Ukrainian S.S. R.,Trans By Rofael, N., Kudus, 157:

AYDOGDU A, OZTURK MO, OGUZ MC and ALTUNEL F. (Received 26. August 2001)

AYDOGDU A, OZTURK MO, OGUZ MC and ALTUNEL F. (Received 26. August 2001) Acta Veterinaria (Beograd), Vol. 51. No. 5-6, 351-358, 2001. UDK 619.639.215.2:616.993 INVESTIGATIONS ON METAZOON PARASITES OF COMMON CARP (Cyprinus carpio L. 1758) IN DALYAN LAGOON, KARACABEY, TURKEY